On seeing the trees and the forest: Single‐signal and multisignal analysis of periictal intracranial EEG

Abstract

Epileptic seizures are associated with a dysregulation of electrical brain activity on many different spatial scales. To better understand the dynamics of epileptic seizures, that is, how the seizures initiate, propagate, and terminate, it is important to consider changes of electrical brain activity on different spatial scales. Herein we set out to analyze periictal electrical brain activity on comparatively small and large spatial scales by assessing changes in single intracranial electroencephalography (EEG) signals and of averaged interdependences of pairs of EEG signals. Single and multiple EEG signals are analyzed by combining methods from symbolic dynamics and information theory. This computationally efficient approach is chosen because at its core it consists of analyzing the occurrence of patterns and bears analogy to classical visual EEG reading. Symbolization is achieved by first mapping the EEG signals into bit strings, that is, long sequences of zeros and ones, depending solely on whether their amplitudes increase or decrease. Bit strings reflect relational aspects between consecutive values of the original EEG signals, but not the values themselves. For each bit string the relative frequencies of the different constituent short bit patterns are then determined and used to compute two information theoretical measures: (1) redundancy (R) of single bit strings characterizes electrical brain activity on a comparatively small spatial scale represented by a single EEG signal and (2) averaged pair-wise mutual information with all other bit strings (M), which allows tracking of larger-scale EEG dynamics. We analyzed 20 periictal intracranial EEG recordings from five patients with pharmacoresistant temporal lobe epilepsy. At seizure onset, R first strongly increased and then decreased toward seizure termination, whereas M gradually increased throughout the seizure. Bit strings with maximal R were always derived from EEG signals recorded from the visually identified seizure-onset zone. When compared to the bit strings derived from other EEG signals, their M was relatively smaller. These findings are consistent with a strong but transient occurrence of information-poor, that is, redundant electrical brain activity on a smaller spatial scale, which is particularly pronounced in the seizure-onset zone. On a larger spatial scale, a progressively more collective state emerges, as revealed by increasing amounts of mutual information. Information theoretical analysis of bit patterns derived from EEG signals helps to characterize periictal brain activity on different spatial scales in a quantitative and efficient way and may provide clinically relevant results.